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Title: Association of pathogen strain-specific gene transcription and transmission efficiency phenotype of Anaplasma marginale

Author
item AGNES, JOSEPH - Washington State University
item Herndon, David
item Ueti, Massaro
item RAMABU, SOLOMON - Washington State University
item EVANS, MARC - Washington State University
item BRAYTON, KELLY - Washington State University
item PALMER, GUY - Washington State University

Submitted to: Infection and Immunity
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/8/2010
Publication Date: 3/22/2010
Citation: Agnes, J.T., Herndon, D.R., Ueti, M.W., Ramabu, S., Evans, M., Brayton, K.A., Palmer, G.H. 2010. Association of pathogen strain-specific gene transcription and transmission efficiency phenotype of Anaplasma marginale. Infection and Immunity. Available: http://iai.asm.org/cgi/reprint/IAI.00108-10v1

Interpretive Summary: The basic requirement for Anaplasma marginale transmission is the ability of the bacteria to infect and replicate within the tick vector. However, the determinants of transmission efficiency by strain-specific differences in transmissibility are largely unknown and represent a significant gap in our knowledge. We used in this study two distinct transmission phenotype strains of Anaplasma marginale. The Saint Maries strain of A. marginale is a prototypical high transmission efficiency strain with replication to high levels in the tick salivary gland and can be transmitted by less than 10 ticks. The Israel vaccine strain (Anaplasma marginale subsp. centrale) is a low transmission efficiency strain and requires 30 fold more tick as compared to the St. Maries strain. In this study we tested whether strain-specific genes expressed in the tick salivary glands at the time of transmission are linked to the differences in transmission efficiency phenotype. We identified 58 strain-specific genes by using both annotation-dependent and independent analyses of the complete genome sequences. Seventeen of the St. Maries strain-specific genes and 18 of those in the Israel vaccine strain were transcribed in the tick salivary gland at the time of transmission. In conclusion, although associated with transmission phenotype, expression levels of strain-specific genes were equal to or less than levels within infected bovine erythrocytes, suggesting that function is not specific to salivary gland colonization.

Technical Abstract: For vector borne pathogens, replication and acquisition of infectiousness within the arthropod vector is required. While the basic lifecycle of development within and transmission from the arthropod vector are known for many bacterial and protozoal pathogens, the determinants of transmission efficiency represented by strain-specific differences in transmissibility are largely unknown and represent a significant gap in our knowledge. The St. Maries strain of Anaplasma marginale is a prototypical high transmission efficiency strain with replication to high titer in the tick salivary gland and can be transmitted by <10 ticks. In contrast, the Israel vaccine strain is representative of low efficiency strains and transmission requires >30 fold more ticks. We hypothesized that strain-specific genes expressed in the tick salivary glands at the time of transmission are linked to the differences in transmission efficiency phenotype. Using both annotation-dependent and independent analyses of the complete genome sequences, we identified 58 strain-specific genes. These strain-specific genes most likely represent divergence from a common ancestral gene in one or both strains based on analysis of synteny and lack of statistical support for acquisition as islands by lateral gene transfer. Seventeen of the St. Maries strain-specific genes and 18 of those in the Israel strain were transcribed in the tick salivary gland at the time of transmission. Although associated with transmission phenotype, expression levels of strain-specific genes were equal to or less than levels within infected erythrocytes in the mammalian host, suggesting that function is not specific to salivary gland colonization.